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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Biochimica et Biophysica Acta 1827 (2013) 145–160 Contents lists available at SciVerse ScienceDirect Biochimica et Biophysica Acta journal homepage: www.elsevier.com/locate/bbabio Review Unifying concepts in anaerobic respiration: Insights from dissimilatory sulfur metabolism☆ Fabian Grein 1, Ana Raquel Ramos, Sofia S. Venceslau, Inês A.C. Pereira ⁎ Instituto de Tecnologia Quimica e Biologica, Universidade Nova de Lisboa, Oeiras, Portugal article info abstract Article history: Behind the versatile nature of prokaryotic energy metabolism is a set of redox proteins having a highly mod- Received 16 July 2012 ular character. It has become increasingly recognized that a limited number of redox modules or building Received in revised form 3 September 2012 blocks appear grouped in different arrangements, giving rise to different proteins and functionalities. This Accepted 4 September 2012 modularity most likely reveals a common and ancient origin for these redox modules, and is obviously Available online 11 September 2012 reflected in similar energy conservation mechanisms. The dissimilation of sulfur compounds was probably one of the earliest biological strategies used by primitive organisms to obtain energy. Here, we review Keywords: Anaerobic respiration some of the redox proteins involved in dissimilatory sulfur metabolism, focusing on sulfate reducing organ- Dissimilatory sulfur metabolism isms, and highlight links between these proteins and others involved in different processes of anaerobic res- Sulfate reducing bacteria piration. Noteworthy are links to the complex iron–sulfur molybdoenzyme family, and heterodisulfide Sulfur oxidizing bacteria reductases of methanogenic archaea. We discuss how chemiosmotic and electron bifurcation/confurcation Redox module may be involved in energy conservation during sulfate reduction, and how introduction of an additional Respiratory membrane complex module, multiheme cytochromes c, opens an alternative bioenergetic strategy that seems to increase meta- bolic versatility. Finally, we highlight new families of heterodisulfide reductase-related proteins from non-methanogenic organisms, which indicate a widespread distribution for these protein modules and may indicate a more general involvement of thiol/disulfide conversions in energy metabolism. This article is part of a Special Issue entitled: The evolutionary aspects of bioenergetic systems. © 2012 Elsevier B.V. All rights reserved. 1. Introduction sulfite) was another possible biological strategy. There is evidence that photosynthetic processes were established at least 3.5 billion The dissimilatory metabolism of sulfur compounds is likely to have years ago [5,6], and dissimilatory sulfur metabolism was also already been among the earliest energy-yielding processes to sustain life [1,2]. present at this time, either as sulfate reduction or sulfur disproportion- In the early anoxic Earth H2SandSO2 wereemittedbyvolcanicand ation, as indicated by sulfur isotope fractionation studies [7–9] and hydrothermal sources, and photolysis of these compounds would also microfossil records [10]. However, this biological activity had little 0 generate elemental sulfur and sulfate [3,4].BothH2SandS could impact on the biogeochemical cycling of sulfur until ~2.45 billion sustain anoxygenic photosynthesis that would produce sulfate, or years ago [11], when a rise in atmospheric oxygen levels (Great Oxida- other oxidized sulfur species, and organic matter. Sulfate and S0 could tion Event) promoted the increase of the oceanic sulfate concentration serve as electron acceptors for H2 oxidation, and disproportionation of from weathering of sulfide minerals on land [12–15].Theincreased S0 and sulfur compounds of intermediate oxidation state (thiosulfate, oxygenation of the atmosphere was likely due to the activity of oxygen-producing cyanobacteria, which seem to have emerged at ap- proximately the same time when O2 started to increase, and much later than once believed [16–18]. The rising O2 promoted weathering of continental pyrite and an increase in oceanic sulfate concentration Abbreviations: SRO, Sulfate reducing organisms; SOB, Sulfur oxidizing bacteria; to low mM levels [12,13,15]. However, for most of the Proterozoic the – LUCA, Last universal common ancestor; CISM, Complex iron sulfur molybdoenzymes; deep ocean waters remained anoxic and sulfidic or ferruginous, overlaid TpIc3, Type I cytochrome c3; TpIIc3, Type II cytochrome c3 – ☆ This article is part of a Special Issue entitled: The evolutionary aspects of bioenergetic by an oxygenated surface layer [12,19 21], a state that may have been systems. perpetuated until as recently as ~600 million years ago by anoxygenic ⁎ Corresponding author at: ITQB/UNL, Av. da Republica‐EAN, 2780‐157 Oeiras, Portugal. photosynthesis with sulfide as electron donor [22]. After a second Tel.: +351 214468327; fax: +351 4469314. major oxidation event in the Neoproterozoic, the deep ocean waters be- E-mail address: [email protected] (I.A.C. Pereira). came oxygenated and the sulfate levels rose to present day levels 1 Presently at Institut für Medizinische Mikrobiologie, Immunologie & Parasitologie, Abteilung Pharmazeutische Mikrobiologie, Rheinische Friedrich-Wilhelms-Universität (28 mM), marking the start of the modern sulfur cycle, where biological Bonn, Bonn, Germany. sulfate reduction plays a major role, particularly in marine sediments 0005-2728/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.bbabio.2012.09.001 Author's personal copy 146 F. Grein et al. / Biochimica et Biophysica Acta 1827 (2013) 145–160 where it is responsible for about 50% of carbon remineralization [23]. high level of gene exchange that was present in the pool of LUCA Overall, it is clear that there was an intimate connection between the organisms [31], as well as the high incidence of lateral gene transfer history of Earth's atmosphere and the biogeochemical cycle of sulfur in later prokaryotes [32]. In sulfur-metabolizing organisms we find in- (reviewed in [24,25]). teresting and unique variations of respiratory proteins that reflect their The start of widespread biological sulfate reduction between 2.45 ancient origin and their close environmental association with other and 2.35 billion years ago is derived from the large increase in anaerobic organisms, in particular with methanogens. Here, we present mass-dependent sulfur isotope fractionations observed during this a short review of respiratory proteins involved in dissimilatory sulfur period (reviewed in [24,26]). A limited incidence of biological sulfate metabolism, focusing on SRO, and discuss new “parts” of the “redox reduction in the very early Earth is also reflected in the fact that this protein construction kit” that are strongly associated with sulfur metabolic trait is not dispersed among prokaryotic organisms, and metabolism but show also links to other respiratory proteins (Fig. 1) might have initially been restricted to some early branching thermo- [33]. We will not discuss several respiratory membrane proteins that philic sulfate reducers. The emergence of mesophilic sulfate reducing are present in SRO, but also in many other classes of prokaryotes, and organisms (SRO) apparently coincided, or shortly followed the thus are not specifically related to sulfur metabolism. A discussion of increase in oceanic sulfate levels [27,28]. This radiation of mesophilic these can be found in [33]. SRO seems to have taken place after the rapid diversification of bacterial lineages observed during the Archaean eon, where a sig- 2. The AprBA and DsrAB terminal reductases and their evolution nificant expansion of energy metabolism genes apparently occurred [29]. There are two biological pathways of sulfate reduction. In the assim- A striking feature of energy metabolism/respiratory proteins is their ilatory pathway, which is widespread in the three domains of life, sulfate modular character, which has been described as being based on a is reduced to sulfide in small amounts and this is transformed into cyste- “redox protein construction kit” [30], from which different combina- ine, from which other biological sulfur-containing molecules are derived tions of a limited number of protein modules originate different protein [34]. In the dissimilatory pathway, which is restricted to five bacterial complexes with diverse physiological functions. This modular charac- and two archaeal lineages, sulfate is the terminal electron acceptor of ter, which is observed in many protein families, denotes a conservative the respiratory pathway producing large quantities of sulfide [35–37]. approach from Nature in using a limited number of original parts to The two pathways (Fig. 2) start with activation of sulfate by reaction derive new metabolic features. However,